Abstract
In order to explore the effect of climate on cattle warble fly infestation, a total of 1.635 animals from 4 departments of Northern Algeria were examined visually and by manual palpation for the presence of warbles. Cattle were examined from March to June 2014, coinciding with the peak of emergence of warbles, and both the prevalence and intensity of infestation were recorded. The departments included in this study were located in the two different climatic areas in Northern Algeria: humid (Bejaia and Tizi Ouzou) and semi-arid (Tissemssilt and Ain Defla). The overall prevalence was 28.75%; the intensity of infestation ranged from 1 to 98 warbles per animal (mean 18.93±11.05). The prevalence and intensity of infestation within the departments with semi-arid climate (38.23%; 21.57±11.98) was significantly higher than in those with humid climate (20.74%; 14.84±7.86). The CHAID algorithm showed the climate as the most influencing factor for warble fly prevalence, followed by the husbandry system and breed. Logistic regression and multivariate ANOVA indicate that in addition to climate, other intrinsic (age, sex, breed) and extrinsic factors (husbandry system, treatment) included in the study also were associated with both, prevalence and intensity of infestation. Our results indicate that in semiarid areas of Northern Algeria environmental conditions are more favorable for the development of free stages (pupae and adult flies) of Hypoderma spp life-cycle than in humid areas.
Keywords: Bovine hypodermosis, Myiasis, Cattle, Climate, Algeria
Cezayir’de Sığır Hipodermosis’in Epidemiyolojisine İklimin Etkisi
Özet
Sığırlarlarda warble sineği (büvelek) istilası üzerine iklimin etkisini ortaya koymak amacıyla, Kuzey Cezayir’in 4 bölgesinden toplam 1.635 hayvan görsel ve el palpasyonuyla büveleklerin varlığı yönünden muayene edildi. Sığırlar büveleklerin ortaya çıkışının zirve (pik) yaptığı Haziran-Mart 2014 arası incelenerek, hem prevalans hem de enfestasyon yoğunluğu kaydedildi. Bu çalışma kapsamındaki bölgeler, Kuzey Cezayir’de iki farklı iklim alanında yer aldı: nemli (Bejaia ve Tizi Ouzou) ve yarı-kurak (Tissemssilt ve Ain Defla). Tüm prevalans %28.75 idi; hayvan başına istila yoğunluğu ise 1 - 98 büvelek arasında değişti (ortalama 18.93±11.05). Yarı-kurak iklime sahip bölgelerdeki yaygınlık ve istila yoğunluğu (%38.23; 21.57±11.98) nemli iklime sahip olanlara göre anlamlı derecede daha yüksek bulundu (%20.74; 14.84±7.86). CHAID algoritması, büvelek sineği prevalansını etkileyen başlıca faktörün iklim olduğunu, diğerlerinin ise yetiştirme sistemi ve ırk olduğunu gösterdi. Lojistik regresyon ve çok değişkenli ANOVA, iklime ek olarak, diğer iç (yaş, cinsiyet, ırk) ve çalışma kapsamındaki dış faktörlerin (yetiştiricilik sistemi, tedavi) hem yaygınlık hem de istila yoğunluğu ile ilişkili olduğunu göstermektedir. Bizim sonuçlarımız; Kuzey Cezayir çevre koşulları altındaki yarı-kurak alanların, Hypoderma spp. yaşam döngüsünün serbest aşamalarının (pupa ve ergin sinek) gelişimi için nemli alanlara göre daha uygun olduğunu göstermektedir.
Anahtar sözcükler: Bovin hipodermozis, Miyazis, Sığır, İklim, Cezayir
Effect of Climate on the Epidemiology of Bovine Hypodermosis
in Algeria
Khelaf SAIDANI
1
Ceferino LÓPEZ-SÁNDEZ
2Pablo DÍAZ-FERNÁNDEZ
2María Patrocinio MORRONDO-PELAYO
2Pablo DÍEZ-BAÑOS
2Ahmed BENAKHLA
3Rosario PANADERO-FONTÁN
21
2
3
Superior National Veterinary School of Algiers Algeria and institute of veterinary sciences, 270 road of Soumaa, Saad Dahleb University, Blida - ALGERIA
Department of Patología Animal (INVESAGA GROUP), Lugo Veterinary Faculty, University of Santiago de Compostela, Lugo - SPAIN
Department of Veterinary Sciences, Faculty of natural and life sciences, University of El-Tarf - ALGERIA
İletişim (Correspondence)
+213 554 209276
kamel_khelaf@yahoo.frINTRODUCTION
Cattle hypodermosis is an obligatory myiasis caused by larvae of Hypoderma bovis and Hypoderma lineatum (Diptera, Oestridae), characterized by the presence of subcutaneous warbles in the dorsal and lumbar region of the animals. For the last 50 years, cattle hypodermosis has represented one of the most significant parasitic diseases in many countries of the northern hemisphere. Warble fly infestation (WFI) greatly impairs livestock production not only by inducing mechanical damage to internal organs (esophagus, spinal column, rumen, lungs) or skin but also by down-regulating the host immune system [1-4].
The biology of Hypoderma is very influenced by weather conditions. Climate directly influences the development of the free stages of the parasite, pupae and adult flies, affecting the chronology of this myiasis and the intensity of infestation [5,6]. Adults are generally active from April to
June in the case of H. lineatum and from mid-June to early September in the case of H. bovis, though precise periods of activity depend on seasonal and geographic differences in climate [7].
Algeria is the second largest country in Africa; it extends from the Mediterranean coastline to the Sahara desert. The slopes of Algeria’s northern mountains and plateaus are used for grazing farming. Cattle are mainly limited to the north of the country with some enclaves elsewhere. Cow’s milk and sheep’s meat are the highest-earning agricultural products for domestic farmers.
Hypodermosis is an underestimated problem in Algeria. Algerian farmers are not aware of the economic losses caused by this parasitic disease and therefore, no specific control measures are undertaken against this myiasis. Moreover, the application of some anthelmintics having ectoparasitic action against Hypoderma spp. (i.e. ivermectin, moxidectin etc.) is widely used in some departments and scarcely employed in others. In Algeria, except the data provided by Benakhla et al.[8] and Benakhla
et al.[9] during the 90s in the North East of the country,
and more recently by Saidani et al.[10] in the North Central
part, not any reliable data are available regarding the epidemiology of this infection. In order to cover this lack of information, the present clinical survey, including departments from humid and semi-arid areas of Algeria, was carried out.
The main objective of this study was to explore the
effects of the climate, on the prevalence and intensity of infection of bovine hypodermosis in Algeria. In addition, our survey could provide some epidemiological data on bovine hypodermosis in the western part of northern Algeria giving that the previous studies on this topic have never covered this area.
MATERIAL and METHODS
Study Area
Northern Algeria is in the temperate zone with a mild Mediterranean climate. However, its broken topography provides sharp local contrasts in both prevailing temperatures and incidence of rainfall. This area is inhabited by more than ninety percent of Algeria´s population, because is the most fertile region in the country. The geographic distribution of cattle, very scarce in southern Algeria, follows almost the same pattern as human inhabitants The present study has been conducted in two bioclimatic areas of northern Algeria (Table 1): in the humid area temperatures are mild and precipitations are around 1.000 mm annually; in contrast, in semi-arid areas differences between high and low temperatures are high and annual rainfall is scarce.
Fig. 1 shows the location of the four Departments included in this study. Two Departments were sampled in the humid area: Bejaia (n=419) and Tizi Ouzou (n=468) and another two in the semi-arid area: Ain Defla (n=325) and Tissemssilt (n=423).
Animals and Sampling
A total of 1.635 animals were randomly examined visually and by manual palpation for the presence of warbles, and both the prevalence and intensity of infestation were recorded.
All the animals were examined at monthly intervals from March to June 2014, which are the months of the year that correspond to the peak of emergence of warble flies in this region. To ovoid false results, neglecting the month effect, all the animals were examined at monthly intervals, and the peak value was taken into account (that of April)
In order to found out the relative distribution of the two species of Hypoderma spp., naturally emerged larvae (n=152; 80 larvae from Tizi Ouzou and 72 from Ain Defla) were collected and preserved in ethanol 70% and subsequently identified by using the morphological keys
Table 1. Mean weather conditions in two climatic areas of northern Algeria (2013) Table 1. Kuzey Cezayir’in iki iklim bölgesindeki ortalama hava koşulları (2013)
Climate Temperature (ºC) Rainfall (mm) Length of Dry Period (month) Relative Humidity (%)
Humid Min: 0-9; Max: 28-31 900-1.200 3-4 79.09
as described by James [11] and Zumpt [12].
Variables were grouped and categorized for statistical analysis as follows:
Age groups: 1 (≤ 12 months-old), 2 (13-36), 3 (>36), Climatic area: 1 (Humid area), 2 (Semi-arid area), Department: 1 (Bejaia), 2 (Tizi Ouzou) in humid area; 3 (Ain Defla), 4 (Tissemssilt) in semi-arid area,
Breed: 0 (Local breed), 1 (Frisian), 2 (Montbéliard), 3 (Flechvieh), 4 (Crossbreed),
Husbandry system: 1 (Intensive), 2 (Semi-extensive), 3 (Extensive),
Sex: 1 (Male), 2 (Female),
Treatment: 0 (Without treatment), 1 (Treated). Statistical Analysis
In order to detect the influence of climate and other intrinsic (age, sex, breed) and extrinsic factors (husbandry system, treatment) in the prevalence of WFI, a Logistic Regression algorithm was applied. The dependent variable was the presence of warbles in each animal. Factors indicated previously were introduced in a backward conditional method and removed from the model one by one (on the basis of the highest p-value) until the best model was built. Next, all pairwise interactions that were biologically plausible were evaluated. Odds ratio
were computed by raising e to the power of the logistic coefficient over the first category of each factor, not over the last.
Chi-squared automatic interaction detector (exhaustive CHAID) has been performed to stratify risk factors in order of importance. CHAID algorithm identified factors that divide cattle in subgroups with different positive/ negative ratio [13]. CHAID is a tool to identify major factors
using as criteria the significance of a Chi-squared test and successively splitting data in increasingly homo-geneous nodes in relation to dependent variable (warble presence) until the classification tree is fully grown.
A multifactorial ANOVA over positive animals was used for the examination of the intensity of infestation; the dependent variable -number of nodules counted in animals- had been previously transformed (squared root of nodules plus 0.5) to normalized the variable. Tukey HSD post hoc test was used to detect the differences between pairs.
Statistical analyses were done using R statistical package v. 3.2.0 [14]. CHAID algorithm was performed with
Answer Tree 3.1 (SPSS Inc., Chicago, IL USA) [10].
RESULTS
In the present study, the overall prevalence was 28.7%. Notable variations in prevalence were observed
Fig 1. Geographic map of Algeria showing
the location of the Departments included in this study
Fig 1. Cezayir’in bu çalışmaya dahil edilen
between the climatic areas (Table 2); the prevalence within the departments with a semi-arid climate was significantly higher than in those with humid climate. Logistic regression (Table 3) indicated that in addition to climate, the other intrinsic (age, sex, breed) and extrinsic factors (husbandry system, treatment) included in the study were associated with warble prevalence
(Table 4). According to this test, cattle in semi-arid areas
have 4.53 times more risk to acquire this myiasis than cattle in humid areas. When considering other factors, Flechvieh cattle have the highest prevalence and local breed the lowest, young animals (≤12 months) are more frequently infested than old animals. The likelihood of being positive is 106.13 times higher in animals kept in an extensive husbandry system than in an intensive system.
Table 2. Prevalence by Hypoderma in cattle from northern Algeria Table 2. Kuzey Cezayir’deki sığırlarda hypoderma prevalansı
Factor Levels ExaminedAnimals Non InfestedAnimals InfestedAnimals Prevalence
Climate Humid 887 703 184 20.74% Semi-arid 748 462 286 38.23% Age <13 months 493 346 147 29.82% 13-36 months 790 552 238 30.12% >36 months 352 267 85 24.14% Sex Male 309 236 73 23.62% Female 1326 929 397 29.94% System Intensive 129 117 12 9.30% Semi-extensive 611 464 147 24.06% Extensive 895 584 311 34.75% Breed Holstein 52 40 12 23.08% Montbéliard 222 165 57 25.68% Fleckvieh 25 5 20 80.00% Crossbreed 572 378 194 33.91% Local breed 764 577 187 24.48% Medication Medicated 769 619 150 19.50% Non-medicated 866 546 320 36.95%
Table 3. Logistic regression results Table 3. Lojistik regresyon sonuçları
Factors Estimate S.E. Z value P OR* Lower Upper95% CI for OR
Climate 1.5112 0.1594 9.481 <0.001 4.53 3.32 6.19 Local breed Freisian breed 2.1550 0.4524 4.763 <0.001 8.63 3.55 20.94 Montbéliard breed 3.4894 0.3251 10.732 <0.001 32.77 17.32 61.97 Flechvieh breed 4.8749 0.5690 8.567 <0.001 130.96 42.93 399.49 Croosbreed 1.3806 0.1675 8.240 <0.001 3.98 2.86 5.52 < 13 months 13-36 months -0.1107 0.1397 -0.793 0.428 0.89 0.68 1.17 > 36 months -0.4271 0.1751 -2.439 0.015 0.65 0.46 0.91 Sex 0.6358 0.2269 2.803 0.005 1.89 1.21 2.95 Intensive system Semi-extensive system 1.8659 0.3754 4.971 <0.001 6.46 3.10 13.49 Extensive system 4.6646 0.5684 8.207 <0.001 106.13 34.84 323.314 Treatment 0.8670 0.4013 2.161 0.031 2.38 1.08 5.22
Table 4. Intensity of infection by Hypoderma spp and statistical result with multifactorial ANOVA Table 4. Hypoderma spp enfeksiyonu yoğunluğu ve çok faktörlü ANOVA ile istatistiksel sonucu
Factors Mean±SD F P Value Factors Mean±SD F P Value
Climate 62.582 < 0.001 Sex 0.080 0.778
Humid 14.84±7.86 Male 16.03±9.76
Semi-arid 21.57±11.98 Female 19.18±11.13
Breed 2.417 0.048 Husbandry system 37.152 < 0.001
Local 20.65±12.96 Intensive 4.67±2.9 Freisian 19.58±7.72* Semi-extensive 14.38±6.55 Montbéliard 13.75±6.68 Extensive 21.64±11.8 Flechvieh 11.6±6.56* Croosbreed 19.52±9.88 Age 16.074 < 0.001 Treatment 24.164 < 0.001 < 13 months 21.67±12.02 No treatment 21.64±11.8 13-36 months 18.5±10.74 Treatment 13.16±6.6 > 36 months 15.41±8.9
Fig 2. Classification tree produced by the CHAID algorithm when considering different factors Fig 2. CHAID algoritmasıyla farklı faktörler dikkate alınarak üretilen sınıflandırma ağacı
The CHAID algorithm showed the climate as the most influencing factor for warble fly prevalence, followed by the husbandry system and breed (Fig. 2).
The intensity of infestation ranged from 1 to 98 warbles per animal (mean 18.9±11.05). As occurred with the prevalence, the lowest intensity was registered in the humid area (Table 3). In addition to climatic area, multifactorial ANOVA also showed significant differences in the intensity of infection when considering the breed and age of the animals; with local breed and young animals showing the highest rates. Management factors like husbandry system and treatment also have a significant influence in the number of warbles/animal.
Out of the 152 identified larvae, 83 (54.5%) were found to belong to Hypoderma lineatum and 69 (45.5%) to H. bovis. Under the humid climate, 47 out of 80 (58.7%) of larvae were H. bovis and the remaining part of H. lineatum. However, in the area from semi arid climate, 50 out of 72 (69.4%) belonged to H. lineatum species (Fig. 3).
DISCUSSION
The overall prevalence of hypodermosis detected in northern Algeria can be considered as moderate (28.7%); this percentage was higher than the 18.1% observed by Saidani et al.[10] in cattle farms from North
Central Algeria and the 3.7% found in an abattoir. How-ever, this prevalence resulted very low as compared to the 76% recorded by Benakhla et al.[9] in the eastern part
of the country.
When considering the department of origin of cattle the lowest prevalence was registered in Bejaia (16.21%), followed by Ain Defla (19.08), Tizi Ouzou (24.79%) and finally, the highest percentage was recorded in Tissemssilt (52.96%). Similarly, as occurred in our survey, Panadero et al.[5] found that Coastal areas, characterized by relatively
high temperatures and by an important summer rainfall,
had the lowest percentages of grub presence, whereas in the interior areas the infestation percentages were higher. The wide variations on prevalence and intensity of infection between humid and semiarid departments could be mainly explained by differences on rainfall and temperature values, as flies generally are not active on dark, cloudy days, at wind velocities above 8m/s, or during periods of rain or snow[15]. However, other
factors affecting the prevalence and intensity of infection might include, breed, husbandry system and the use of insecticides [16-19]. Indeed, Chi-squared automatic interaction
detector (exhaustive CHAID) revealed the climate as the most important factor followed by the management system and breed. The husbandry system is known to exert a major effect on both prevalence and intensity of bovine hypodermosis since the free grazing system is the most favorable for the occurrence of this myiasis, under which flies have more chances to contact the animal. This fact agrees with several previous studies [5,10,16-19].
Surprisingly, in this study local breeds mainly kept under extensive and semi-extensive husbandry systems showed the lowest prevalence but the highest parasite burdens. Moreover, multifactorial ANOVA and logistic regression also identified the use of drugs (avermectins) as a factor influencing, the intensity and prevalence of infection.
Both the prevalence and the intensity of bovine hypodermosis differ significantly from one area to another. It is usual to notice a wide variation in the prevalence of WFI among different parts of the world and even within the same country[16]. This variability might be due to
the differences in the climatic factors that affect the developmental stages of the larvae [5,20]. Consequently,
the lower prevalence and intensity recorded in the area from humid climate can be explained by the high relative humidity and rainfall, which are harmful to the free stages of warble flies according to Tarry[20]. Ahmed et
al.[18] found that the high level of infestation were due to
the climatic conditions, location, treatment procedures, topography of the area and extensive grazing. Despite
Fig 3. Monthly evolution of H. bovis and H. lineatum in
two climatic areas in northern Algeria
Fig 3. Kuzey Cezayir’de iki iklim bölgesindeki H. bovis
the moderate prevalence found in this study especially in Bejaia and Tizi Ouzou departments, the burden of infestation is generally heavy (up to 98 larvae), which indicate that the implementation of a control program for hypodermosis in Algeria is very indispensable.
In our survey, H. bovis and H. lineatum were found infesting cattle, although there was a slight predominance of H. lineatum (54.5%). This statement agrees with previous findings in the same country[10,21]. The identification of
the species of Hypoderma implicated in a given area is of vital importance for several reasons. Firstly because H. bovis is currently believed to affect only cattle living in the Northern countries, and secondly because the impact of H. bovis on animal welfare and health is more important than H. lineatum due to the fact that if treatments are not carried out promptly, when first stage larvae are still in the peri-rachidian channel, paralysis of the hind quarters may occur. This finding is of relevance for the correct use of drugs against hypodermosis [22].
Thirdly, Hypoderma bovis is more harmful and frighten the host several times during laying because its eggs are glued singly on the flank or lower abdomen while Hypoderma lineatum lays in groups of 5 to 15 eggs onto the hair of the forelegs, breast or underside of the body [1], thus it causes
less fear. It is thus obvious that the severity of gadding is different according to the Hypoderma species.
As regard to the distribution of the two species, our results were in accordance with what was found by Benakhla et al.[9], where the 2 species of genus Hypoderma
were present in cattle in Algeria (H. bovis and H. lineatum) with a predominance of H. lineatum (63%) in the semi- arid area and a majority of H. bovis (75%) in humid area. Warbles appeared and disappeared earlier in the semi- arid area. Indeed, in the present study no larva was found in the semi arid area since the end of May. During March, Hypoderma lineatum was predominant in both climatic areas, which is in favor of the early emergence of this species [8,9]. The peak of emergence was reached
during April regardless to the species, similarly as recorded for the 1635 animals clinically examined. On May, H. lineatum was slightly more frequent. Finally, on June the larvae collected exclusively from humid climatic with of a majority of Hypoderma bovis (Fig. 3). This finding is once more in agreement to previous studies on this topic, where the warbles disappear one month later in humid area [8].
As conclusion, climatic area was identified as a significant factor affecting the percentage of positive animals and the intensity of parasitation by Hypoderma sp. Our results indicate that in semiarid areas of Northern Algeria environmental conditions are more favorable for the development of free stages (pupae and adult flies) of Hypoderma spp life-cycle than humid areas. However, the climate does not exert its effect alone, others intrinsic
and extrinsic factors such as grazing pattern, breed and medication were also involved on the epidemiology of warble fly infestation.
A
cknowledgementsThis work was partially supported by a grant to K. Saidani (PNE2014/2015 MESRS Algérie) and by a grant for Consolidating and Structuring competitive research groups (R2014/005, Xunta de Galicia, Spain)
c
onflictofi
nterestThe authors declare that they have no conflict of interest.
REFERENCES
1. Scholl PJ: The current situation of hypodermosis in North America. In, Boulard C, Sol J, O’Brien D, Webster K, Sampimon OC (Eds): COST 811
Improvements in the Control Methods for Warble Fly in Livestock. 38-41, European Commission, Brussels, 1998.
2. Tarry DW: Biology, economic effects, and early efforts to eradicate
Hypoderma. In, Boulard C, Sol J, Pithan K, O’Brien D, Webster K, Sampimon OC (Eds): Improvements in the Control Methods for Warble Fly in Livestock. 13-17, Brussels, COST 811, European Commission, 1998.
3. Boulard C: Durably controlling bovine hypodermosis. Vet Res, 33, 455-464, 2002.
4. Panadero R, Dacal V, López C, Vázquez L, Cienfuegos S, Díaz P, Morrondo P, Díez Baños P: Immunomodulatory effect of Hypoderma
lineatum antigens: In vitro effect on bovine lymphocyteproliferation
and cytokine production. Parasite Immunol, 31, 72-77, 2009. DOI: 10.1111/j.1365-3024.2008.01072.x
5. Panadero R, López C, Díez N, Paz A, Díez P, Morrondo P: Influence of internal and environmental factors on the distribution and occurrence of
Hypoderma (Diptera: Oestridae) in cattle in Galicia (Northwest of Spain). J Med Entomol, 37, 27-28, 2000. DOI: 10.1603/0022-2585-37.1.27
6. Panadero R, Vazquez L, Colwell, DD, Lopez C, Dacal V, Morrondo P, Diez-Banos P: Evaluation of an antigen captures ELISA for the early diagnosis of Hypoderma lineatum in cattle under field conditions. Vet
Parasitol, 147, 297-302, 2007. DOI: 10.1016/j.vetpar.2007.04.004
7. Colebrook E, Wall R: Ectoparasites of livestock in Europe and the Mediterranean region. Vet Parasitol, 120, 251-274, 2004. DOI: 10.1016/j. vetpar.2004.01.012
8. Benakhla A, Boulard C, Sedraqui S, Oussaid F: L’hypodermose bovine: Approche épidémiologique et caractérisation du cycle biologique en vue de l’établissement d’un plan de prophylaxie dans le nord est Algérien. Rev Med Vet, 144, 693-700, 1993.
9. Benakhla A, Lonneux JF, Mekroud A, Losson B, Boulard C: Hypodermose bovine dans le Nord-Est algérien: Prévalence et intensité d’infestation. Vet Res, 30, 539-545, 1999.
10. Saidani K, López C, Mekademi K, Díaz P, Díez-Baños P, Benakhla A, Panadero R: Bovine hypodermosis in North-central Algeria: Prevalence, intensity of infection and risk factors. Kafkas Univ Vet Fak Derg, 20, 871-876, 2014. DOI: 10.9775/kvfd.2014.11197
11. James TM: The flies that cause myiasis in man. United State
Department of Agriculture Miscellaneous Publication, 631, 175, 1947.
12. Zumpt F: Myiasis in Man and Animals in the Old World. Butterworth,
London, 205-229, 1965.
13. Lopez C, Fernandez M, Cienfuegos M, Panadero R, Vázquez L, Díaz P, Pato J, Lago N, Dacal V, Díez-Baños P, Morrondo P: Protostrongylid infection in meat sheep from Northwestern Spain: Prevalence and risk factors. Vet Parasitol, 31, 108-114, 2011. DOI: 10.1016/j.vetpar.2010.12.038 14. R Core Team R: A language and environment for statistical computing.
R foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org, 2015.
15. Anderson JR, Nilssen AC, Folstad I: Mating behavior and thermoregulation of the reindeer warble fly, Hypoderma tarandi L. (Diptera: Oestridae). J Insect Behav 7, 679-706, 1994. DOI: 10.1007/ BF01997439
16. Khan MN, Iqbal Z, Sajid MS, Anwar M: Bovine hypodermosis: Prevalence and economic significance in Southern Punjab, Pakistan. Vet
Parasitol, 141, 386-390, 2006. DOI: 10.1016/j.vetpar.2006.05.014
17. Zalla P, Shoshi N, Bejo B, Postoli R, Rapti D: Impact of management system on the presence of hypodermosis in cattle. Maced J Anim Sci, 2 (2): 235-240, 2012.
18. Ahmed H, Khan MR, Panadero R, Lopez C, Asif S., Irfan M, Mazhar Q: Influence of epidemiological factors on the prevalence and intensity
of infestation by Hypoderma spp. (Diptera: Oestidae) in cattle of Potowar Region, Pakistan. Pakistan J Zool, 45 (6): 1495-1500, 2013.
19. Ahmed H, Khan MR, Panadero R, López C, Iqbal MF, Naqvi SMS, Qayum M: Geographical distribution of Hypodermosis (Hypoderma sp.) in Northern Punjab, Pakistan. Kafkas Univ Vet Fak Derg, 18 (Suppl-A): A215-A219, 2012. DOI: 10.9775/kvfd.2012.6533
20. Tarry D: Warble fly infestation and climate. Vet Res, 106, 559-560, 1980. DOI: 10.1136/vr.106.26.559
21. Saidani K, Benakhla A, Díez-Baños P, Panadero R: Chronobiology of Hypoderma spp. in North-central Algeria as a basis to establish a control program. Rev Ibero-Latinoam Parasitol, 70 (2): 157-162, 2011.
22. Otranto D, Zalla P, Testini G, Zanaj S: Cattle grub infestation by
Hypoderma sp. in Albania and risks for European countries. Vet Parasitol,
